Tobacco pollen tubes – a fast and easy tool for studying lipid droplet association of plant proteins

Plant Journal

Volumn 89, Issue 5, 2017, Pages 1055-1064

  Müller, Anna Ophelia ^a   Blersch, Katharina Franziska ^a   Gippert, Anna Lena ^a   Ischebeck, Till ^a  

^a UNIVERSITY OF GÖTTINGEN   (Germany)

Author keywords

Arabidopsis thaliana; Chlamydomonas reinhardtii; lipid droplets; Nicotiana tabacum; Physcomitrella patens; pollen tubes; protein localization; technical advance; transient transformation

Indexed keywords

CYTOLOGY; DIGITAL STORAGE; DROPS; PLANTS (BOTANY); TOBACCO;

ARABIDOPSIS THALIANA; CHLAMYDOMONAS REINHARDTII; LIPID DROPLETS; NICOTIANA TABACUM; PHYSCOMITRELLA PATENS; POLLEN TUBE; PROTEIN LOCALIZATION; TECHNICAL ADVANCES;

PROTEINS;

PLANTS; PROTEINS; STORAGE;

FAT DROPLET; PLANT PROTEIN;

ARABIDOPSIS; BRYOPSIDA; CHLAMYDOMONAS REINHARDTII; GENETIC TRANSFORMATION; GENETICS; METABOLISM; POLLEN TUBE; TOBACCO;

ARABIDOPSIS; BRYOPSIDA; CHLAMYDOMONAS REINHARDTII; LIPID DROPLETS; PLANT PROTEINS; POLLEN TUBE; TOBACCO; TRANSFORMATION, GENETIC;

EID: 85013175519     PISSN: 09607412     EISSN: 1365313X     Source Type: Journal    
DOI: 10.1111/tpj.13441     Document Type: Article

References (49)

1. Athenstaedt, K. and Daum, G. (2003) YMR313c/TGL3 encodes a novel triacylglycerol lipase located in lipid particles of Saccharomyces cerevisiae. J. Biol. Chem. 278, 23317–23323.
2. Beller, M., Bulankina, A.V., Hsiao, H.-H., Urlaub, H., Jäckle, H. and Kühnlein, R.P. (2010) PERILIPIN-dependent control of lipid droplet structure and fat storage in Drosophila. Cell Metab. 12, 521–532.
3. Bewley, J.D., Bradford, K., Hilhorst, H. and Nonogaki, H. (2013) Seeds: Physiology of Development, Germination and Dormancy, 3rd edn. New York: Springer-Verlag. ISBN: 978-1-4614-4693-4.
4. Cai, Y., Goodman, J.M., Pyc, M., Mullen, R.T., Dyer, J.M. and Chapman, K.D. (2015) Arabidopsis SEIPIN proteins modulate triacylglycerol accumulation and influence lipid droplet proliferation. Plant Cell, 27, 2616–2636.
5. Chapman, K.D., Dyer, J.M. and Mullen, R.T. (2012) Biogenesis and functions of lipid droplets in plants. J. Lipid Res. 53, 215–226.
6. Dracopoli, N.C., Haines, J.L. and Korf, B.R. (1994) Current Protocols in Human Genetics. New York: John Wiley & Sons.
7. Eastmond, P.J. (2006) SUGAR-DEPENDENT1 encodes a patatin domain triacylglycerol lipase that initiates storage oil breakdown in germinating Arabidopsis seeds. Plant Cell, 18, 665–675.
8. Feraru, E. and Friml, J. (2008) PIN polar targeting. Plant Physiol. 147, 1553–1559.
9. Fu, C., Wehr, D.R., Edwards, J. and Hauge, B. (2008) Rapid one-step recombinational cloning. Nucleic Acids Res. 36, e54.
10. Fulda, M., Shockey, J., Werber, M., Wolter, F.P. and Heinz, E. (2002) Two long-chain acyl-CoA synthetases from Arabidopsis thaliana involved in peroxisomal fatty acid β-oxidation. Plant J. 32, 93–103.
11. Gidda, S.K., Park, S., Pyc, M., Yurchenko, O., Cai, Y., Wu, P., Andrews, D.W., Chapman, K.D., Dyer, J.M. and Mullen, R.T. (2016) Lipid Droplet-Associated Proteins (LDAPs) are required for the dynamic regulation of neutral lipid compartmentation in plant cells. Plant Physiol. 170, 2052–2071.
12. Green, M. and Sambrook, J. (2012) Molecular Cloning: A Laboratory Manual. New York: Cold Spring Harbor Laboratory Press.
13. Grillitsch, K., Connerth, M., Köfeler, H., Arrey, T.N., Rietschel, B., Wagner, B., Karas, M. and Daum, G. (2011) Lipid particles/droplets of the yeast Saccharomyces cerevisiae revisited: lipidome meets proteome. Biochim. Biophys. Acta, 1811, 1165–1176.
14. Grippa, A., Buxó, L., Mora, G., Funaya, C., Idrissi, F.-Z., Mancuso, F., Gomez, R., Muntanyà, J., Sabidó, E. and Carvalho, P. (2015) The seipin complex Fld1/Ldb16 stabilizes ER–lipid droplet contact sites. J. Cell Biol. 211, 829–844.
15. Gronke, S., Mildner, A., Fellert, S., Tennagels, N., Petry, S., Muller, G., Jackle, H. and Kuhnlein, R.P. (2005) Brummer lipase is an evolutionary conserved fat storage regulator in Drosophila. Cell Metab. 1, 323–330.
16. Honys, D. and Twell, D. (2004) Transcriptome analysis of haploid male gametophyte development in Arabidopsis. Genome Biol. 5, R85.
17. Horn, P.J., James, C.N., Gidda, S.K., Kilaru, A., Dyer, J.M., Mullen, R.T., Ohlrogge, J.B. and Chapman, K.D. (2013) Identification of a new class of lipid droplet-associated proteins in plants. Plant Physiol. 162, 1926–1936.
18. Huang, A.H.C. (1992) Oil bodies and oleosins in seeds. Annu. Rev. Plant Physiol. Plant Mol. Biol. 43, 177–200.
19. Ischebeck, T., Stenzel, I. and Heilmann, I. (2008) Type B phosphatidylinositol-4-phosphate 5-kinases mediate Arabidopsis and Nicotiana tabacum pollen tube growth by regulating apical pectin secretion. Plant Cell, 20, 3312–3330.
20. James, C.N., Horn, P.J., Case, C.R., Gidda, S.K., Zhang, D., Mullen, R.T., Dyer, J.M., Anderson, R.G.W. and Chapman, K.D. (2010) Disruption of the Arabidopsis CGI-58 homologue produces Chanarin-Dorfman-like lipid droplet accumulation in plants. Proc. Natl Acad. Sci. 107, 17833–17838.
21. Jiang, P.L. and Tzen, J.T. (2010) Caleosin serves as the major structural protein as efficient as oleosin on the surface of seed oil bodies. Plant Signal Behav, 5, 447–449.
22. Jiang, P.-L., Jauh, G.-Y., Wang, C.-S. and Tzen, J.T.C. (2008) A unique caleosin in oil bodies of lily pollen. Plant Cell Physiol. 49, 1390–1395.
23. Jolivet, P., Roux, E., d'Andrea, S., Davanture, M., Negroni, L., Zivy, M. and Chardot, T. (2004) Protein composition of oil bodies in Arabidopsis thaliana ecotype WS. Plant Physiol. Biochem. 42, 501–509.
24. Jolivet, P., Boulard, C., Bellamy, A., Larre, C., Barre, M., Rogniaux, H., d'Andrea, S., Chardot, T. and Nesi, N. (2009) Protein composition of oil bodies from mature Brassica napus seeds. Proteomics, 9, 3268–3284.
25. Jolivet, P., Boulard, C., Bellamy, A., Valot, B., d'Andréa, S., Zivy, M., Nesi, N. and Chardot, T. (2011) Oil body proteins sequentially accumulate throughout seed development in Brassica napus. J. Plant Physiol. 168, 2015–2020.
26. Kim, H.U., Hsieh, K., Ratnayake, C. and Huang, A.H. (2002) A novel group of oleosins is present inside the pollen of Arabidopsis. J. Biol. Chem. 277, 22677–22684.
27. Kost, B., Spielhofer, P. and Chua, N.H. (1998) A GFP-mouse talin fusion protein labels plant actin filaments in vivo and visualizes the actin cytoskeleton in growing pollen tubes. Plant J., 16, 393–401.
28. Krenek, P., Samajova, O., Luptovciak, I., Doskocilova, A., Komis, G. and Samaj, J. (2015) Transient plant transformation mediated by Agrobacterium tumefaciens: principles, methods and applications. Biotechnol. Adv. 33, 1024–1042.
29. Lee, H.-I., Gal, S., Newman, T.C. and Raikhel, N.V. (1993) The Arabidopsis endoplasmic reticulum retention receptor functions in yeast. Proc. Natl Acad. Sci. USA, 90, 11433–11437.
30. Li-Beisson, Y. and Peltier, G. (2013) Third-generation biofuels: current and future research on microalgal lipid biotechnology. OCL, 20, D606.
31. Liu, H., Wang, C., Chen, F. and Shen, S. (2015) Proteomic analysis of oil bodies in mature Jatropha curcas seeds with different lipid content. J. Proteomics. 113, 403–414.
32. Mähs, A., Steinhorst, L., Han, J.P., Shen, L.K., Wang, Y. and Kudla, J. (2013) The calcineurin B-like Ca2 + sensors CBL1 and CBL9 function in pollen germination and pollen tube growth in Arabidopsis. Mol Plant, 6, 1149–1162.
33. Moellering, E.R. and Benning, C. (2010) RNA interference silencing of a major lipid droplet protein affects lipid droplet size in Chlamydomonas reinhardtii. Eukaryot. Cell, 9, 97–106.
34. Negrutiu, I., Shillito, R., Potrykus, I., Biasini, G. and Sala, F. (1987) Hybrid genes in the analysis of transformation conditions. Plant Mol. Biol. 8, 363–373.
35. Nelson, B.K., Cai, X. and Nebenfuhr, A. (2007) A multicolored set of in vivo organelle markers for co-localization studies in Arabidopsis and other plants. Plant J. 51, 1126–1136.
36. Nguyen, H.M., Baudet, M., Cuine, S. et al. (2011) Proteomic profiling of oil bodies isolated from the unicellular green microalga Chlamydomonas reinhardtii: with focus on proteins involved in lipid metabolism. Proteomics, 11, 4266–4273.
37. Read, S., Clarke, A. and Bacic, A. (1993) Stimulation of growth of culturedNicotiana tabacum W 38 pollen tubes by poly (ethylene glycol) and Cu (II) salts. Protoplasma, 177, 1–14.
38. Scott, A., Wyatt, S., Tsou, P.L., Robertson, D. and Allen, N.S. (1999) Model system for plant cell biology: GFP imaging in living onion epidermal cells. Biotechniques, 26(1125), 1128–1132.
39. Steinhorst, L., Mahs, A., Ischebeck, T., Zhang, C., Zhang, X., Arendt, S., Schultke, S., Heilmann, I. and Kudla, J. (2015) Vacuolar CBL-CIPK12 Ca(2 +)-sensor-kinase complexes are required for polarized pollen tube growth. Curr. Biol. 25, 1475–1482.
40. Szymanski, K.M., Binns, D., Bartz, R., Grishin, N.V., Li, W.P., Agarwal, A.K., Garg, A., Anderson, R.G. and Goodman, J.M. (2007) The lipodystrophy protein seipin is found at endoplasmic reticulum lipid droplet junctions and is important for droplet morphology. Proc Natl Acad Sci U S A, 104, 20890–20895.
41. Taylor, N.J. and Fauquet, C.M. (2002) Microparticle bombardment as a tool in plant science and agricultural biotechnology. DNA Cell Biol. 21, 963–977.
42. Taylor, R.G., Walker, D.C. and McInnes, R. (1993) E. coli host strains significantly affect the quality of small scale plasmid DNA preparations used for sequencing. Nucleic Acids Res. 21, 1677.
43. Tsai, C.-H., Zienkiewicz, K., Amstutz, C.L., Brink, B.G., Warakanont, J., Roston, R. and Benning, C. (2015) Dynamics of protein and polar lipid recruitment during lipid droplet assembly in Chlamydomonas reinhardtii. Plant J. 83, 650–660.
44. Twell, D., Yamaguchi, J., Wing, R.A., Ushiba, J. and McCormick, S. (1991) Promoter analysis of genes that are coordinately expressed during pollen development reveals pollen-specific enhancer sequences and shared regulatory elements. Genes Dev. 5, 496–507.
45. Vance, V.B. and Huang, A.H.C. (1987) The major protein from lipid bodies of maize. J. Biol. Chem. 262, 11275–11279.
46. Vermachova, M., Purkrtova, Z., Santrucek, J., Jolivet, P., Chardot, T. and Kodicek, M. (2011) New protein isoforms identified within Arabidopsis thaliana seed oil bodies combining chymotrypsin/trypsin digestion and peptide fragmentation analysis. Proteomics, 11, 3430–3434.
47. Walther, T.C. and Farese, R.V. Jr (2012) Lipid droplets and cellular lipid metabolism. Annu. Rev. Biochem. 81, 687–714.
48. Wanner, G., Formanek, H. and Theimer, R.R. (1981) The ontogeny of lipid bodies (spherosomes) in plant cells. Planta, 151, 109–123.
49. Wydro, M., Kozubek, E. and Lehmann, P. (2006) Optimization of transient Agrobacterium-mediated gene expression system in leaves of Nicotiana benthamiana. Acta Biochim. Pol. 53, 289–298.